Nucleotide P2Y1 receptor regulates EGF receptor mitogenic signaling and expression in epithelial cells

Journal of Cell Science

Volumn 120, Issue 24, 2007, Pages 4289-4301

  Buvinic, Sonja ^a,b   Bravo Zehnder, Marcela ^a,b,c   Boyer, José Luis ^d,e   Huidobro Toro, Juan Pablo ^a,b   González, Alfonso ^a,b,c  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b UNIVERSIDAD ANDRÉS BELLO   (Chile)

^c PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^e MERCK RESEARCH LABORATORIES   (United States)

Author keywords

EGFR; Epithelia; GPCR; Nucleotides; Proliferation; Transactivation

Indexed keywords

ADENOSINE DIPHOSPHATE; EPIDERMAL GROWTH FACTOR RECEPTOR; G PROTEIN COUPLED RECEPTOR; NUCLEOTIDE; PURINERGIC P2Y1 RECEPTOR; ADENOSINE TRIPHOSPHATE; CALCIUM; DRUG DERIVATIVE; N(6) METHYL 2' DEOXYADENOSINE 3',5' DIPHOSPHATE; N(6)-METHYL-2'-DEOXYADENOSINE 3',5'-DIPHOSPHATE; PURINERGIC P2 RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CANCER GROWTH; CELL PROLIFERATION; CELL STRAIN; EPITHELIUM CELL; GENE EXPRESSION REGULATION; HELA CELL; HUMAN; MITOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; ANIMAL; CELL LINE; CYTOLOGY; DOG; DRUG POTENTIATION; FISCHER 344 RAT; GENETIC TRANSFECTION; GENETICS; METABOLISM; RAT; TRANSACTIVATION;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM; CELL LINE; CELL PROLIFERATION; DOGS; EPITHELIAL CELLS; HELA CELLS; HUMANS; RATS; RATS, INBRED F344; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, PURINERGIC P2; SIGNAL TRANSDUCTION; TRANS-ACTIVATION (GENETICS); TRANSFECTION;

EID: 38349046982     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.03490     Document Type: Article

References (90)

1. Arteaga, C. L. (2002). Epidermal growth factor receptor dependence in human tumors: more than just expression? Oncologist 7 Suppl. 4, 31-39.
2. Bjorge, J. D. and Kudlow, J. E. (1987). Epidermal growth factor receptor synthesis is stimulated by phorbol ester and epidermal growth factor. Evidence for a common mechanism. J. Biol. Chem. 262, 6615-6622.
3. Bjorge, J. D., Paterson, A. J. and Kudlow, J. E. (1989). Phorbol ester or epidermal growth factor (EGF) stimulates the concurrent accumulation of mRNA for the EGF receptor and its ligand transforming growth factor-alpha in a breast cancer cell line. J. Biol. Chem. 264, 4021-4027.
4. Bravo-Zehnder, M., Orio, P., Norambuena, A., Wallner, M., Meera, P., Toro, L., Latorre, R. and Gonzalez, A. (2000). Apical sorting of a voltage- and Ca2+-activated K+ channel alpha-subunit in Madin-Darby canine kidney cells is independent of N-glycosylation. Proc. Natl. Acad. Sci. USA 97, 13114-13119.
5. Burrell, H. E., Wlodarski, B., Foster, B. J., Buckley, K. A., Sharpe, G. R., Quayle, J. M., Simpson, A. W. and Gallagher, J. A. (2005). Human keratinocytes release ATP and utilize three mechanisms for nucleotide interconversion at the cell surface. J. Biol. Chem. 280, 29667-29676.
6. Buvinic, S., Poblete, I., Donoso, V., Delpiano, A. M., Briones, R., Miranda, R. and Huidobro-Toro, J. P. (2006). P2Y1 and P2Y2 receptor distribution varies along the human placenta vascular tree; a role of nucleotides in vascular tone regulation. J. Physiol. 573, 427-443.
7. Cardona, C., Rabbitts, P. H., Spindel, E. R., Ghatei, M. A., Bleehen, N. M., Bloom, S. R. and Reeve, J. G. (1991). Production of neuromedin B and neuromedin B gene expression in human lung tumor cell lines. Cancer Res. 51, 5205-5211.
8. Carpenter, G. (1999). Employment of the epidermal growth factor receptor in growth factor-independent signaling pathways. J. Cell Biol. 146, 697-702.
9. Carpenter, G. (2000). EGF receptor transactivation mediated by the proteolytic production of EGF-like agonists. Sci STKE 2000, PE1.
10. Coussens, L. M. and Werb, Z. (2002). Inflammation and cancer. Nature 420, 860-867.
11. Cuttitta, F., Carney, D. N., Mulshine, J., Moody, T. W., Fedorko, J., Fischler, A. and Minna, J. D. (1985). Autocrine growth factors in human small cell lung cancer. Cancer Surv. 4, 707-727.
12. Daub, H., Weiss, F. U., Waliasch, C. and Ullrich, A. (1996). Role of transactivation of the EGF receptor in signalling by G-protein-coupled receptors. Nature 379, 557-560.
13. Daub, H., Wallasch, C., Lankenau, A., Herrlich, A. and Ullrich, A. (1997). Signal characteristics of G protein-transactivated EGF receptor. EMBO J. 16, 7032-7044.
14. Dhanasekaran, N., Tsim, S. T., Dermott, J. M. and Onesime, D. (1998). Regulation of cell proliferation by G proteins. Oncogene 17, 1383-1394.
15. Dong, J., Opresko, L. K., Dempsey, P. J., Lauffenburger, D. A., Coffey, R. J. and Wiley, H. S. (1999). Metalloprotease-mediated ligand release regulates autocrine signaling through the epidermal growth factor receptor. Proc. Natl. Acad. Sci. USA 96, 6235-6240.
16. Dong, J., Opresko, L. K., Chrisler, W., Orr, G., Quesenberry, R. D., Lauffenburger, D. A. and Wiley, H. S. (2005). The membrane-anchoring domain of epidermal growth factor receptor ligands dictates their ability to operate in juxtacrine mode. Mol. Biol. Cell 16, 2984-2998.
17. Earp, H. S., Hepler, J. R., Petch, L. A., Miller, A., Berry, A. R., Harris, J., Raymond, V. W., McCune, B. K., Lee, L. W., Grisham, J. W. et al. (1988). Epidermal growth factor (EGF) and hormones stimulate phosphoinositide hydrolysis and increase EGF receptor protein synthesis and mRNA levels in rat liver epithclial cells. Evidence for protein kinase C-dependent and -independent pathways. J. Biol. Chem. 263, 13868-13874.
18. Erlinge, D. (1998). Extracellular ATP: a growth factor for vascular smooth muscle cells. Gen. Pharmacol. 31, 1-8.
19. Goishi, K., Higashiyama, S., Klagsbrun, M., Nakano, N., Umata, T., Ishikawa, M., Mekada, E. and Taniguchi, N. (1995). Phorbol ester induces the rapid processing of cell surface heparin-binding EGF-like growth factor: conversion from juxtacrine to paracrine growth factor activity. Mol. Biol. Cell 6, 967-980.
20. Gschwind, A., Zwick, E., Prenzel, N., Leserer, M. and Ulbrich, A. (2001). Cell communication networks: epidermal growth factor receptor transactivation as the paradigm for interreceptor signal transmission. Oncogene 20, 1594-1600.
21. Gschwind, A., Fischer, O. M. and Ulbrich, A. (2004). The discovery of receptor tyrosine kinases: targets for cancer therapy. Nat. Rev. Cancer 4, 361-370.
22. Guerrero, J., Santibanez, J. F., Gonzalez, A. and Martinez, J. (2004). EGF receptor transactivation by urokinase receptor stimulus through a mechanism involving Src and matrix metalloproteinases. Exp. Cell Res. 292, 201-208.
23. Gutkind, J. S. (1998). Cell growth control by G protein-coupled receptors: from signal transduction to signal integration. Oncogene 17, 1331-1342.
24. Gutkind, J. S., Novotny, E. A., Brann, M. R. and Robbins, K. C. (1991). Muscarinic acetylcholine receptor subtypes as agonist-dependent oncogenes. Proc. Natl. Acad. Sci. USA 88, 4703-4707.
25. Hackel, P. O., Zwick, E., Prenzel, N. and Ullrich, A. (1999). Epidermal growth factor receptors: critical mediators of multiple receptor pathways. Curr. Opin. Cell Biol. 11, 184-189.
26. He, C., Hobert, M., Friend, L. and Carlin, C. (2002). The epidermal growth factor receptor juxtamembrane domain has multiple basolateral plasma membrane localization determinants, including a dominant signal with a polyprohne core. J. Biol. Chem. 277, 38284-38293.
27. Heasley, L. E. (2001). Autocrine and paractme signaling through neuropeptide receptors in human cancer. Oncogene 20, 1563-1569.
28. Hutchings, S. E. and Sato, G. H. (1978). Growth and maintenance of HeLa cells in serum-free medium supplemented with hormones. Proc. Natl. Acad. Sci. USA 75, 901-904.
29. Izumi, Y., Hirata, M., Hasuwa, H., Iwamoto, R., Umata, T., Miyado, K., Tamai, Y., Kurisaki, T., Sehara-Fujisawa, A., Ohno, S. et al. (1998). A metalloprotease-disintegrin, MDC9/meltrin-gamma/ADAM9 and PKCdelta are involved in TPA-induced ectodomain shedding of membrane-anchored heparin-binding EGF-Iike growth factor. EMBO J. 17, 7260-7272.
30. Janssens, R., Communi, D., Pirotton, S., Samson, M., Parmentier, M. and Boeynaems, J. M. (1996). Cloning and tissue distribution of the human P2Y1 receptor. Biochem. Biophys. Res. Commun. 221, 588-593.
31. Jones, S. M. and Kaziauskas, A. (2001a). Growth factor-dependent signaling and cell cycle progression. Chem. Rev. 101, 2413-2423.
32. Jones, S.M.and Kazlauskas, A. (2001b). Growth-factor-dependent mitogenesis requires two distinct phases of signalling. Nat. Cell Biol. 3, 165-172.
33. Jorissen, R. N., Walker, F., Pouliot, N., Garrett, T. P., Ward, C. W. and Burgess, A. W. (2003). Epidermal growth factor receptor: mechanisms of activation and signalling. Exp. Cell Res. 284, 31-53.
34. Julius, D., Livelli, T. J., Jessell, T. M. and Axel, R. (1989). Ectopic expression of the serotonin Ic receptor and the triggering of malignant transformation. Science 244, 1057-1062.
35. Kris, R. M., Lax, L, Gullick, W., Waterfield, M. D., Ullrich, A., Fridkin, M. and Schlessinger, J. (1985). Antibodies against a synthetic peptide as a probe for the kinase activity of the avian EGF receptor and v-erbB protein. Cell 40, 619-625.
36. Lazarowski, E. R., Boucher, R. C. and Harden, T. K. (2003). Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules. Mol. Pharmacol. 64, 785-795.
37. Lazarowski, E. R., Tarran, R., Grubb, B. R., van Heusden, C. A., Okada, S. and Boucher, R. C. (2004). Nucleotide release provides a mechanism for airway surface liquid homeostasis. J. Biol. Chem. 279, 36855-36864.
38. Leipziger, J. (2003). Control of epithelial transport via luminal P2 receptors. Am. J. Physiol. Renal Physiol. 284, F419-F432.
39. Li, S., Huang, S. and Peng, S. B. (2005). Overexpression of G protein-coupled receptors in cancer cells: involvement in tumor progression. Int. J. Oncol. 27, 1329-1339.
40. Liu, J., Liao, Z., Camden, J., Griffin, K. D., Garrad, R. C., Santiago-Perez, L. I., Gonzalez, F. A., Seye, C. I., Weisman, G. A. and Erb, L. (2004). Src homology 3 binding sites in the P2Y2 nucleotide receptor interact with Src and regulate activities of Src, proline-rich tyrosine kinase 2, and growth factor receptors. J. Biol. Chem. 279, 8212-8218.
41. Margolis, B., Li, N., Koch, A., Mohammadi, M., Hurwitz, D. R., Zilberstein, A., Ullrich, A., Pawson, T. and Schlessinger, J. (1990). The tyrosine phosphorylated carboxyterminus of the EGF receptor is a binding site for GAP and PLC-gamma. EMBO J. 9, 4375-4380.
42. Marin, Y. E. and Chen, S. (2004). Involvement of metabotropic glutamate receptor 1, a G protein coupled receptor, in melanoma development. J. Mol. Med. 82, 735-749.
43. Marinissen, M. J. and Gutkind, J. S. (2001). G-protein-coupled receptors and signaling networks: emerging paradigms. Trends Pharmacol. Sci. 22, 368-376.
44. Marmor, M. D., Skaria, K. B. and Yarden, Y. (2004). Signal transduction and oncogenesis by ErbB/HER receptors. Int. J. Radiat. Oncol. Biol. Phys. 58, 903-913.
45. Massague, J. and Pandiella, A. (1993). Membrane-anchored growth factors. Annu. Rev. Biochem. 62, 515-541.
46. Miettinen, P. J., Berger, J. E., Meneses, J., Phung, Y., Pedersen, R. A., Werb, Z. and Derynck, R. (1995). Epithelial immaturity and multiorgan failure in mice lacking epidermal growth factor receptor. Nature 376, 337-341.
47. Mishra, S. K., Braun, N., Shukla, V., Fullgrabe, M, Schomerus, C., Korf, H. W., Gachet, C., Ikehara, Y., Sevigny, J., Robson, S. C. et al. (2006). Extracellular nucleotide signaling in adult neural stem cells: synergism with growth factor-mediated cellular proliferation. Development 133, 675-684.
48. Moore, D., Chambers, J., Waldvogel, H., Faull, R. and Emson, P. (2000). Regional and cellular distribution of the P2Y(1) purinergic receptor in the human brain: striking neuronal localisation. J. Comp. Neurol. 421, 374-384.
49. Morris, J. B., Pham, T. M., Kenney, B., Sheppard, K. E. and Woodcock, E. A. (2004). UTP transactivates epidermal growth factor receptors and promotes cardiomyocyte hypertrophy despite inhibiting transcription of the hypertrophic marker gene, atrial natriuretic peptide. J. Biol. Chem. 279, 8740-8746.
50. Nandigama, R., Padmasekar, M., Wartenberg, M. and Sauer, H. (2006). Feed forward cycle of hypotonic stress-induced ATP release, purinergic receptor activation, and growth stimulation of prostate cancer cells. J. Biol. Chem. 281, 5686-5693.
51. Neary, J. T., Kang, Y., Bu. Y., Yu, E., Akong, K. and Peters, C. M. (1999). Mitogenic signaling by ATP/P2Y purinergic receptors in astrocytes: involvement of a calcium-independent protein kinase C, extracellular signal-regulated protein kinase pathway distinct from the phosphatidylinositol-specific phospholipase C/calcium pathway. J. Neurosci. 19, 4211-4220.
52. Parnot, C., Miserey-Lenkei, S., Bardin, S., Corvol, P. and Clauser, E. (2002). Lessons from constitutively active mutants of G protein-coupled receptors. Trends Endocrinol. Metab. 13, 336-343.
53. Pennock, S. and Wang, Z. (2003). Stimulation of cell proliferation by endosomal epidermal growth factor receptor as revealed through two distinct phases of signaling. Mol. Cell. Biol. 23, 5803-5815.
54. Peto, J. (2001). Cancer epidemiology in the last century and the next decade. Nature 411, 390-395.
55. Pollock, P. M., Cohen-Solal, K., Sood, R., Namkoong, J., Martino, J. J., Koganti, A., Zhu, H., Robbins, C., Makalowska, I., Shin, S. S. et al. (2003). Melanoma mouse model implicates metabotropic glutamate signaling in melanocytic neoplasia. Nat. Genet. 34, 108-112.
56. Polo, S. and Di Fiore, P. P. (2006). Endocytosis conducts the cell signaling orchestra. Cell 124, 897-900.
57. Prenzel, N., Zwick, E., Daub, H., Leserer, M., Abraham, R., Wallasch, C. and Ullrich, A. (1999). EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 402, 884-888.
58. Ralevic, V. and Burnstock, G. (1998). Receptors for purines and pyrimidines. Pharmacol. Rev. 50, 413-492.
59. Rice, W. R., Burton, F. M. and Fiedeldey, D. T. (1995). Cloning and expression of the alveolar type II cell P2u-purinergic receptor. Am. J. Respir. Cell Mol. Biol. 12, 27-32.
60. Sak, K. and Webb, T. E. (2002). A retrospective of recombinant P2Y receptor subtypes and their pharmacology. Arch. Biochem. Biophys. 397, 131-136.
61. Salazar, G. and Gonzalez, A. (2002). Novel mechanism for regulation of epidermal growth factor receptor endocytosis revealed by protein kinase A inhibition. Mol. Biol. Cell 13, 1677-1693.
62. Schafer, B., Marg, B., Gschwind, A. and Ullrich, A. (2004). Distinct ADAM metalloproteinases regulate G protem-coupled receptor-induccd cell proliferation and survival. J. Biol. Chem. 279, 47929-47938.
63. Schafer, R., Sedehizade, F., Welte, T. and Reiser, G. (2003). ATP- and UTP-activated P2Y receptors differently regulate proliferation of human lung epithelial tumor cells. Am. J. Physiol. Lung Cell Mol. Physiol. 285, L376-L385.
64. Schlessinger, J. (2000). Cell signaling by receptor tyrosine kinases. Cell 103, 211-225.
65. Schlessinger, J. (2002). Ligand-induced, receptor-mediated dimerization and activation of EGF receptor. Cell 110, 669-672.
66. Schwiebert, E. M. and Zsembery, A. (2003). Extracellular ATP as a signaling molecule for epithelial cells. Biochim. Biophys. Acta 1615, 7-32.
67. Shechter, Y., Hernaez, L. and Cuatrecasas, P. (1978). Epidermal growth factor: biological activity requires persistent occupation of high-affinity cell surface receptors. Proc. Natl. Acad. Sci. USA 75, 5788-5791.
68. Sibilia, M. and Wagner, E. F. (1995). Strain-dependent epithelial defects in mice lacking the EGF receptor. Science 269, 234-238.
69. Singh, A. B., Tsukada, T., Zent, R. and Harris, R. C. (2004). Membrane-associated HB-EGF modulates HGF-induced cellular responses in MDCK cells. J. Cell Sci. 117, 1365-1379.
70. Soltoff, S. P. (1998). Related adhesion focal tyrosine kinase and the epidermal growth factor receptor mediate the stimulation of mitogen-activated protein kinase by the G-protein-coupled P2Y2 receptor. Phorbol ester or [Ca2+]i elevation can substitute for receptor activation. J. Biol. Chem. 273, 23110-23117.
71. Soltoff, S. P., Avraham, H., Avraham, S. and Cantley, L. C. (1998). Activation of P2Y2 receptors by UTP and ATP stimulates mitogen-activated kmase activity through a pathway that involves related adhesion focal tyrosine kinase and protein kinase C. J. Biol. Chem. 273, 2653-2660.
72. Threadgill, D. W., Długosz, A. A., Hansen, L. A., Tennenbaum, T., Lichti, U., Yee, D., LaMantia, C., Mourton, T., Herrup, K., Harris, R. C. et al. (1995). Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science 269, 230-234.
73. Todorov, L. D., Mihaylova-Todorova, S., Craviso, G. L., Bjur, R. A. and Westfall, D. P. (1996). Evidence for the differential release of the cotransmitters ATP and noradrenaline from sympathetic nerves of the guinea-pig vas deferens. J. Physiol. 496, 731-748.
74. Tornquist, K., Ekokoski, E. and Dugue, B. (1996). Purinergic agonist ATP is a comitogen in thyroid FRTL-5 cells. J. Cell. Physiol. 166, 241-248.
75. Tsai, W., Morielli, A. D. and Peralta, E. G. (1997). The m1 muscarinic acetylcholine receptor transactivates the EGF receptor to modulate ion channel activity. EMBO J. 16, 4597-4605.
76. Tu, M. T., Luo, S. F., Wang, C. C., Chien, C. S., Chiu, C. T., Lin, C. C. and Yang, C. M. (2000). P2Y(2) receptor-mediated proliferation of C(6) glioma cells via activation of Ras/Raf/MEK/MAPK pathway. Br. J. Pharmacol. 129, 1481-1489.
77. Van Kolen, K., Gilany, K., Moens, L., Esmans, E. L. and Slegers, H. (2006). P2Y(12) receptor signalling towards PKB proceeds through IGF-I receptor cross-talk and requires activation of Src, Pyk2 and Rap1. Cell. Signal. 18, 1169-1181.
78. von Kugelgeu, I. (2006). Pharmacological profiles of cloned mammalian P2Y-receptor subtypes. Pharmacol. Ther. 110, 415-432.
79. Wagstaff, S. C., Bowler, W. B., Gallagher, J. A. and Hipskind, R. A. (2000). Extracellular ATP activates multiple signalling pathways and potentiates growth factor-induced c-fos gene expression in MCF-7 breast cancer cells. Carcinogenesis 21, 2175-2181.
80. Wang, D. J., Huang, N. N. and Heppel, L. A. (1992). Extracellular ATP and ADP stimulate proliferation of porcine aortic smooth muscle cells. J. Cell. Physiol. 153, 221-233.
81. Wetzker, R. and Bohmer, F. D. (2003). Transactivation joins multiple tracks to the ERK/MAPK cascade. Nat. Rev. Mol. Cell Biol. 4, 651-657.
82. Whitehead, I., Kirk, H. and Kay, R. (1995). Expression cloning of oncogenes by retroviral transfer of cDNA libraries. Mol. Cell. Biol. 15, 704-710.
83. Wiley, H. S. (2003). Trafficking of the ErbB receptors and its influence on signaling. Exp. Cell Res. 284, 78-88.
84. Wolff, S. C., Qi, A. D., Harden, T. K. and Nicholas, R. A. (2005). Polarized expression of human P2Y receptors in epithelial cells from kidney, lung, and colon. Am. J. Physiol. Cell Physiol. 288, C624-C632.
85. Van, Y., Shirakabe, K. and Werb, Z. (2002). The metalloprotease Kuzbanian (ADAM10) mediates the transactivation of EGF receptor by G protein-coupled receptors. J. Cell Biol. 158, 221-226.
86. Yarden, Y. (2001). The EGFR family and its ligands in human cancer. signalling mechanisms and therapeutic opportunities. Eur. J. Cancer 37 Suppl. 4, S3-S8.
87. Yarden, Y. and Sliwkowski, M. X. (2001). Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2, 127-137.
88. Yerxa, B. R., Sabater, J. R., Davis, C. W., Stutts, M. J., Lang-Furr, M., Picher, M., Jones, A. C., Cowlen, M., Dougherty, R., Boyer, J. et al. (2002). Pharmacology of INS37217 [P(1)-(uridine 5′)-P(4)-(2′-deoxycytidine 5′)tetraphosphate, tetrasodium. salt], a next-generation P2Y(2) receptor agonist for the treatment of cystic fibrosis. J. Pharmacol. Exp. Ther. 302, 871-880.
89. Yu, S. M., Chen, S. F., Lau, Y. T., Yang, C. M. and Chen, J. C. (1996). Mechanism of extracellular ATP-induced proliferation of vascular smooth muscle cells. Mol. Pharmacol. 50, 1000-1009.
90. Zwick, E., Wallasch, C., Daub, H. and Ullrich, A. (1999). Distinct calcium-dependent pathways of epidermal growth factor receptor transactivation and PYK2 tyrosine phosphorylation in PC12 cells. J. Biol. Chem. 274, 20989-20996.